Shifted levels of sleep and activity during the night as mechanisms underlying ectoparasite resistance.

npj Biological Timing and Sleep Pub Date : 2025-01-01 Epub Date: 2025-04-02 DOI:10.1038/s44323-025-00031-7
Joshua B Benoit, Joy Bose, Oluwaseun M Ajayi, Ashley Webster, Karl Grieshop, David Lewis, Hailie Talbott, Michal Polak
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Abstract

Parasites harm host fitness and are pervasive agents of natural selection capable of driving the evolution of host resistance traits. Previously we demonstrated evolutionary responses to artificial selection for increasing behavioral immunity to Gamasodes queenslandicus mites for Drosophila melanogaster. Here, we report transcriptional shifts in metabolic processes due to selection for mite resistance. We also show decreased starvation resistance and increased use of nutrient reserves in flies from mite-resistant lines. Resistant lines exhibited increased activity, reduced sleep, and elevated oxygen consumption during the night. Using a panel of D. melanogaster lines exhibiting variable sleep durations, we found a positive correlation between mite resistance and reduced sleep. Restraining the activity of artificially selected mite-resistant flies during exposure to parasites reduced their resistance advantage relative to control flies. The results suggest that ectoparasite resistance in this system involves increased activity during the scotophase and metabolic gene expression at the expense of starvation resistance.

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夜间睡眠和活动水平的变化是抵抗外寄生虫的机制。
寄生虫危害宿主的适应性,是普遍存在的自然选择因子,能够推动宿主抗性性状的进化。在此之前,我们证明了黑腹果蝇对人工选择的进化反应,以增加对昆士兰革螨的行为免疫。在这里,我们报告了代谢过程中的转录变化,这是由于螨虫抗性的选择。我们还发现,来自抗螨系的果蝇对饥饿的抵抗力下降,对营养储备的利用增加。抗性品系表现出活动增加、睡眠减少和夜间耗氧量升高。利用一组睡眠时间不同的黑腹田鼠,我们发现抗螨性和睡眠减少之间存在正相关关系。在暴露于寄生虫时,抑制人工选择的抗螨蝇的活性会降低其相对于对照蝇的抗性优势。结果表明,该系统的外寄生虫抗性包括在寄生期增加活性和代谢基因表达,以牺牲饥饿抗性为代价。
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